05. ADHERENCE_01. Interacción 11/06/14 14:09 Página 989
Nutr Hosp. 2014;29(5):989-996 ISSN 0212-1611 • CODEN NUHOEQ S.V.R. 318
Revisión
Adherence to Mediterranean diet and bone health Antonio Romero Pérez1 y Ana Rivas Velasco2 Servicio Andaluz de Salud. Spain. 2Departamento de Nutrición y Bromatología. Facultad de Farmacia. Universidad de Granada. Spain.
1
Abstract Introduction: Several studies have concluded that incidences of osteoporosis and osteoporosis-related fractures vary across the European Union, the lowest incidence being reported in the Mediterranean area. The beneficial effect is mainly attributed to a specific eating pattern. The Mediterranean diet contain a complex array of naturally occurring bioactive molecules with antioxidant, anti-inflammatory and alkalinising properties that may contribute to the bone-sparing effect of the Mediterranean diet. Objective: The purpose of this review is to examine the evidence to date on the effects of Mediterranean diet on bone health. Methods: The search for articles came from extensive research in the following databases: PubMed, Scopus and Web of Science. We used the search terms “Mediterranean diet”, “adherence”, “fruit and vegetable“, “olive oil“, “fish” “legume”, “cereal” “alcohol”, “bone”, “osteoporosis”, “fracture”, and combinations, such as “Mediterranean diet and bone” or “Mediterranean diet and fracture”. Results: A limited number of studies have examined the relationship between Mediterranean Diet and bone health, and they have reported conflicting results. On the one hand, adherence to a traditional MeDi has been associated with higher bone mineral density and lower fracture risk. The results of these studies could be attributed to the combined beneficial effects of individual components of the Mediterranean diet. On the contrary, several studies failed to show any association between adherence to the MeDi and indices of bone mass. Conclusions: Further large-scale studies are required to clarify the effect of Mediterranean diet on bone health, in order to establish the role of this diet in the prevention of osteoporosis.
(Nutr Hosp. 2014;29:989-996) DOI:10.3305/nh.2014.29.5.7332 Key words: Mediterranean diet. Osteoporosis. Bone.
ADHERENCIA A LA DIETA MEDITERRÁNEA Y SALUD ÓSEA Resumen Introducción: Se han encontrado diferencias en los valores de incidencia de osteoporosis y fracturas relacionadas entre los países de la Unión Europea, siendo menor en los países de la zona mediterránea. Este hecho se atribuye principalmente a un patrón de alimentación específica común. La dieta mediterránea contiene un complejo conjunto de componentes bioactivos con propiedades antioxidantes, anti-inflamatorias y alcalinizantes que pueden contribuir al efecto de esta dieta en la salud ósea. Objetivo: El propósito de esta revisión es examinar la evidencia hasta la fecha sobre los efectos de la dieta mediterránea sobre la salud ósea. Métodos: Se realizó una búsqueda en la literatura científica utilizando las siguientes base de datos: PubMed, Scopus and Web of Science. Utilizamos los términos de búsqueda “Dieta Mediterránea”, “adhesión“, “frutas y verduras”, “aceite de oliva“, “pescado” “legumbres”, “cereal”, “alcohol”, “hueso“, “osteoporosis”,”fractura”, y combinaciones, como “Dieta Mediterránea y el hueso“ o “Dieta mediterránea y fracturas“. Resultados: Existe un número limitado de estudios que analicen la relación entre el seguimiento de la Dieta Mediterránea y la salud ósea, mostrando resultados contradictorios. Diversos trabajos han mostrado que la adherencia a una dieta mediterránea tradicional se asociado con una mayor densidad mineral ósea y un menor riesgo de fractura en población adulta. Los resultados de estos estudios podrían atribuirse a un efecto beneficioso combinado de los componentes individuales de la dieta mediterránea. Por el contrario, en otros trabajos no se ha encontrado ninguna asociación entre la adherencia a la dieta mediterránea y los índices de masa ósea. Conclusiones: Se requieren más estudios a gran escala para aclarar el efecto de la dieta mediterránea sobre la salud ósea, con el fin de establecer el papel de la dieta en la prevención de la osteoporosis.
(Nutr Hosp. 2014;29:989-996) DOI:10.3305/nh.2014.29.5.7332 Correspondence: Ana Rivas Velasco. Departamento de Nutrición y Bromatología. Facultad de Farmacia. Universidad de Granada. E-mail: [email protected]
Palabras clave: Dieta mediterránea. Osteoporosis. Hueso.
Recibido: 7-II-2014. 1.ª Revisión: 11-II-2014. Aceptado: 12-III-2014.
989
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 990
Introduction Osteoporosis (OP) is an important worldwide public health concern1 that affects many millions of people around the world and that will take on increasing significance as people live longer and the world s population continues to increase in number2. In addition, osteoporosis related fractures are one of the leading causes of significant morbidity and disability in elderly patients and increases the economic burden on the health care system.The mechanisms involved in osteoporosis pathogenesis are not fully understood3. A reduction in bone density in earlier life is likely to increase the risk of OP and its sequelae in adulthood. It is therefore important to raise awareness among the general population on the need to form and maintain good bone health from childhood through the adoption of healthy habits. OP development is influenced by multiple factors. Bone modelling and remodelling processes are governed not only by heritable traits but also by nutritional, mechanical and hormonal factors4. Besides the aging process, an inadequate diet and sedentary lifestyle can reduce mineralization. Although nutrition is only one of the many factors that influence bone mass and fragility fractures, it is of particular importance to bone health because it is modifiable. Diet can be modified for the maintenance and development of bone mass. Proper nutrient intake has a crucial role in both prevention and treatment of osteoporosis5. The most relevant nutrients to bone health are calcium and phosphorus because they compose roughly 80% to 90% of the mineral content of bone hydroxyapatite; protein is essential because it is incorporated into the organic matrix of bone for collagen structure upon which mineralization occurs; trace elements, and vitamins (e.g., vitamins D and K) are also crucial in carrying out metabolic processes and reactions in bone6,7. Other benefits on bone metabolism derives from bioactive components found basically in vegetables but also some herbs and fruit. Phytochemicals, antioxidants, and other bioactive compounds influence bone metabolism through a variety of mechanisms mainly in reducing oxidative stress and inflammation8. To date, the most consistently followed approach to examine the potential relation between dietary factors and skeletal health was based on particular nutrients such as calcium and vitamin D3. However, people do not eat isolated nutrients but meals consisting of a variety of foods with complex combinations of nutrients and bioactive components. The traditional analysis considering the effect of a few isolated nutrients on bone health misses a lot of information regarding complex or cumulative correlations and interactions between these compounds contained in food. For this reason, there is an increasing interest in the study of dietary patterns that could answer some questions and promote the development of appropriate recommendations for overall dietary habits9 .
990
Nutr Hosp. 2014;29(5):989-996
Several studies have concluded that incidences of osteoporosis and osteoporosis-related fractures vary across the European Union. Conspicuous differences are encountered in the severity of osteoporosis, the lowest incidence being reported in the Mediterranean area10. The beneficial effect is mainly attributed to a specific eating pattern. The Mediterranean diet (MeDi) key characteristics are high intake of vegetables, legumes, fruits and cereals; moderate to high intake of fish; low intake of saturated lipids and high intake of unsaturated lipids, particulary olive oil; low to moderate intake of dairy products, low intake of meat; and modest intake of ethanol, mostly in the form of wine11,12. The Mediterranean diet was introduced to the scientific community by the classic Seven Countries study. Since then data on the association between this diet and cardiovascular disease13,14, cancer and other chronic diseases have been accumulating15,16. However, a limited number of cross-sectional studies have examined the relationship between Mediterranean diet adherence and bone health, and they have reported conflicting results. Therefore, the purpose of this review is to examine the evidence to date on the effects of Mediterranean diet on bone health. Methods The search for articles came from extensive research in the following databases: PubMed, Scopus and Web of Science. We used the search terms “Mediterranean diet”, “adherence”, “fruit and vegetable“, “olive oil“, “fish” “legume”, “cereal” “alcohol”, “bone”, “osteoporosis”, “fracture”, and combinations, such as “Mediterranean diet and bone” or “Mediterranean diet and fracture”. The titles and abstracts of the located documents were initially reviewed and the reference lists of selected papers were searched to identify additional articles. We narrowed the search to studies published in English. Additional publications were identified from references provided in original papers. Results and discussion Adherence to Mediterranean diet and bone health The Mediterranean diet is characterized by a high intake of olive oil, plant products, fish and seafood; a low intake of dairies, meat and meat products; and a moderate ethanol intake15. These food items contain a complex array of naturally occurring bioactive molecules with antioxidant, anti-inflammatory and alkalinising properties that may contribute to the bone-sparing effect of the Mediterranean diet10. Adherence to a dietary pattern close to the Mediterranean diet, have shown to prevent bone disease. Eating habits based on fruit, vegetables, milk, and cereals –that is, similar to those of the Mediterranean
Antonio Romero Pérez and Ana Rivas Velasco
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 991
diet– were proven by the Framingham study to be significantly associated with greater bone mass17. Nakashima and Takayanagi18 studied associations between dietary patterns and bone mineral density in Japanese farmwomen and showed that a “healthy” pattern, described by high intakes of green and dark yellow vegetables, mushrooms, fish and shellfish, and fruit, was positively related to bone mineral density. Furthermore, the effect of vegetarian dietary patterns on skeletal health has been studied; lacto-ovo vegetarians appear to have normal bone mass when compared with omnivores. However, a more recent study reported that the scientific findings support the hypothesis that vegans do have lower bone mineral density than their nonvegan counterparts19. There are few studies that have assessed the effect of the Mediterranean diet on bone health. Besides, the impact of MeDi adherence on bone health remains unclear. In table I are summarized the characteristics of these studies included in relation to where the work was conducted, the number of participants in each study, the methods used to evaluate Mediterranean diet adherence, and the main results. Kontogianni et al.20 described that adherence to a Mediterranean diet evaluated through a Mediterranean Diet Score was not associated with bone mass rates in a sample of adult Greek women, whereas adherence to a dietary pattern close to the Mediterranean diet, i.e., high consumption of fish and olive oil and low red meat intakes, was positively related to bone mass, suggesting the potential bonepreserving properties of this pattern through adult life. An interventional study conducted in Spain21, concluded that a Mediterranean dietary pattern enriched with mixed nuts, does not seem to have any significant effect on bone metabolism in elderly subjects. However the authors pointed out that the sample selection criteria could limit the extrapolation of the findings, as the endpoint of the study was cardiovascular mortality, so the study focused on subjects with a high risk of cardiovascular disease and had already been eating a reasonably good Mediterranean diet pattern for a long time before randomization into the trial21. Recently, Rivas and coworkers22 hypothesized that adherence to the Mediterranean diet measured as a Mediterranean diet score (MDS) has a beneficial effect on bone mineral density in the calcaneus measured by a dual energy X-ray absorptiometry. For the purposes of this study, a sample of healthy women from Southern Spain was chosen. Subjects were grouped into two major groups: a first group consisted of women of reproductive age, and a second group consisted of postmenopausal women. Significant linear trends between the MDS and bone mineral density were observed in all subjects studied. The authors concluded that a varied diet based on Mediterranean diet patterns may be beneficial in the prevention of osteoporosis. Fernandez-Real et al.23 compared the effects of a virgin olive oil enriched Mediterranean diet, a walnut-enriched Mediterranean diet, and a low-
Adherence to Mediterranean diet and bone health
fat diet for two years on osteocalcin and bone formation markers in the blood of men at high risk of cardiovascular disease. The virgin olive oil enriched Mediterranean diet alone was associated with increased serum levels of osteocalcin and the bone remodelling marker procollagen amino-terminal propeptide, suggesting a protective role for this diet in bone health. The potential protective effect of the MeDi against the risk of hip fractures has been evaluated in several studies. Recently, in a large cohort of adults from eight European countries, Benetou et al11 reported an inverse association between adherence to a Mediterraneantype diet and the risk of hip fracture in European older persons. Indeed, in this large cohort of adults enrolled in the EPIC study (N = 188,795 participants, 802 incident hip fractures), higher adherence to the MeDi was associated with a 7% decrease in hip fracture incidence, notably among participants aged 60 years or older and among men in the model adjusted only. On the contrary Feart and coworkers24 showed that greater MeDi adherence was not associated with a decreased risk of fractures in French older persons. There is evidence that specific components of Mediterranean diet may prevent the prevention of osteoporosis and/or hip fracture occurrence. In this context, a summary of the studies that demonstrate this association is shown below. Olive oil and bone Scarce epidemiological literature is available about the association between fat intake and the bone health. Saturated fat (SFA) intake has been reported to be associated with a higher risk of bone loss and osteoporotic fractures25. On the contrary, monounsaturated fat (MUFA) has been reported to have a beneficial effect on bone health25,26. Various epidemiological studies have associated the intake of the monounsaturated fatty acids of olive oil with bone health. A study of male and female adults in Greece26 reported a positive association between the intake of monounsaturated fats and mineral bone density; the authors highlighted the substantially lower incidence of fractures in Greece, where there is high olive oil consumption, than in the USA or North European countries. Rivas et al.4 described in female adults in Spain a significant correlation between the consumption of monounsaturated fatty acids and the mineral density of the heel bone (calcaneus). Besides triglycerides, olive oil contains a wide variety of so-called minor compounds that are of major importance from a chemical and organoleptic standpoint. These include phenolic compounds, which constitute a highly complex fraction formed by numerous substances, some of which are yet to be identified. The known substances include simple phenols, e.g., hydroxytyrosol, tyrosol, caffeic acid, vanillic acid, p-coumaric acid, ferulic acid, and vanillin; flavonoids,
Nutr Hosp. 2014;29(5):989-996
991
992
Nutr Hosp. 2014;29(5):989-996 Adult aged 60 to 80 years at high risk for CVdisease (N=230).
Adult women aged 18-65 years (N=200).
Fernández-real et al. (2012) 23 Spain.
Rivas et al. (2013)22
Method used to evaluate MeDi adherence Results
Mediterranean Diet Score Significant linear trends (Trichopoulou et al., 2003) 22. between MeDi adherence and BMD were observed (p= 0.001).
Three interventional groups: Total osteocalcin increased in the MedDiet+VOO group (p=0.007) low-fat diet, a MedDi in parallel to increased P1NP levels (p=0.01) but not in subjects supplemented with VOO, on the MedDiet+nuts (p=0.32). or MedDi supplemented with nuts.
Three interventional groups: Subjects in MedDi with nuts group had nonsignificantly higher urine low-fat diet, a MedDi free deoxypyridoxine:creatinine ratio (p=0.14). supplemented with VOO, or MedDi supplemented with nuts.
France
Adult aged 67 years Incidence of hip, vertebral and wrist fractures Mediterranean Diet Score Higher MeDi adherence was associated with a non-significant or older (N=1,482). were self-reported every 2 years over 8 years. (Trichopoulou et al., 2003)22. increased risk of fractures at any site.
European Adults aged 35-70 years Incident hip fracture was reported by hip Mediterranean Diet Score Adherence to MeDi was associated with a 7% decrease in hip countries (N= 188,795). and radius fracture registries for a median (Trichopoulou et al., 2003)22. fracture incidence. Association was more evident among men and participants in the of 9 years. older individuals. EPIC study.
Calcaneous BMD by DEXA.
Total circulating osteocalcin Bone markers N-terminal propeptide (P1NP).
Bone formation and resorption markers Bone mass by ultrasound scanning.
MeDi: Mediterranean diet. BMD: bone mineral density. DEXA: Dual-energy X-ray absorptiometry. CV: cardiovascular. VOO: Virgin olive oil.
Feart et al. (2013)24
Benetou et al. (2013)11
Adult aged 60 to 80 at high risk for CVdisease (N=230).
Spain.
Bullo et al. (2009) 21
Spain.
Method for measuring bone mass/fracture risk
Conclusions
Greater MeDi adherence was not associated with a decreased risk of fractures in French older persons.
Increased adherence to MeDi appears to protect against hip fracture occurrence, particularly among men.
MedDi pattern is associated with higher BMD.
Consumption of a Mediterranean diet enriched with virgin olive oil for 2 years is associated with increased serum osteocalcin and P1NP concentrations, suggesting protective effects on bone.
A Mediterranean dietary pattern does not seem to have a much greater effect on bone metabolism biomarker.
Adult women (N=300) Lumbar spine and total BMD by DEXA. Mediterranean Diet Score Adherence to MedDi was not associated with indices of bone mass. Adherence to a MedDi was not associated (Trichopoulou et al., 2003) 22. Consumption of fish, olive oil and low intake of red meat was associated with indices of bone mass. with lumbar spine BMD (p = 0.017) and total body BMD (p = 0.048)
Subjects
Greece.
Country
Kontogani et al. (2010)20
Reference
Tabla I Description of the studies that have assessed the effect of the Mediterranean diet on bone health
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 992
Antonio Romero Pérez and Ana Rivas Velasco
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 993
e.g., luteolin and apigenin; and other more complex compounds such as those derived from oleuropein, ligstroside, ligustaloside27. Numerous potential health benefits of the phenolic compounds of olive oil have been reported, but their role in the prevention of bone diseases (e.g., osteoporosis) has been less well studied. Researchers have shown the phenolic compounds in different vegetables species can modulate the functions of osteoblastic cells, including their proliferative capacity and maturation, by increasing alkaline phosphatase activity and the deposit of calcium ions in the extracellular matrix28-30. Oleuropein, the main phenolic compound in olive-tree leaves, together with virgin olive oil and olives, was proved to be effective in a rat model of senile osteoporosis with a dosage of 150 mg/kg diet. In addition oleuropein shifts the differentiation of mesenchymal stromal cells in favour of osteoblastogenesis suggesting that oleuropein intake might have preventive effects against the bone loss associated with osteoporosis and aging31. The main phenolic compounds in virgin olive oil are tyrosol and hydroxytyrosol. Their administration in the diet at doses of 0.017% prevented the inflammation-induced bone mass loss in ovariectomized rats in a model of senile osteoporosis and increased their osteoblast activity, as evidenced by their elevated plasma osteocalcin levels32,33. Finally, luteolin, a flavonoid present in VOO, lessens bone mass loss in postmenopausal osteoporosis by reducing osteoclast differentiation and function34. Intake of fruits and vegetables: implications for bone health Fruit and vegetable consumption is a common feature of the Mediterranean diet. Recent studies have focused on the effects of fruit and vegetable intakes on bone health35,36. Fruit and vegetable intake has been associated with increased bone mineral density or reduced fracture risk37. Larger bone size in early pubertal children and adolescents38-40, and better bone mass in adult men and women have been associated with fruit and vegetable consumption41,42. In addition, it has been demonstrated that a dietary intervention based on low fat and increased fruit, vegetable, and grain intake reduced moderately the risk of multiple falls and slightly lower hip BMD43. The mechanism whereby fruit and vegetables may affect bone is not clear and may be multifactorial44. Fruits and vegetables might affect bone health via the effects of several components in these foods, such as minerals (e.g., calcium, potassium, and magnesium), vitamins (e.g., vitamin K and C), phytochemicals (e.g., phytoestrogens), and oligosaccharides (especially inulin-type fructans), either through their effect on calcium absorption or their involvement in the bone remodeling sequence, could mediate this association11,45. In addition, fruits and vegetables contain many
Adherence to Mediterranean diet and bone health
different antioxidant components. Several lines of evidence suggest a tight association between oxidative stress and the pathogenesis of osteoporosis in humans. It has been shown that osteoporotic women have lower serum antioxidants levels as compared with controls12,46. Recently, Rivas et al.3 demonstrated that the overall dietary antioxidant intake was significantly associated with bone mineral density in adult women. It should be taken into account that a higher dietary acid load is believed to result in bone mineral dissolution and greater bone resorption, and a diet rich in fruit and vegetables may result in a more alkaline environment, which has been proven to reduce urinary calcium excretion43. The low grade metabolic acidosis induced by the modern diet is exacerbated during ageing when renal function begins to decline requiring the body’s skeletal reserves to be called upon to relinquish bicarbonate to produce alkaline buffers needed to continuously balance the acid load.Typical diets are acidic because predominantly acid (hydrogen ions) rather than base (bicarbonate) is created during the metabolism of the daily food intake. Acid forming grains and high protein food derived from animal origin (meat, fish, and eggs) contain sulphur-based amino acids, methionine, and cysteine which create acid when metabolized. Alkaline forming foods contain potassium salts which can be broken down to make alkaline buffers47. Fruit/vegetables influence on acid-base balance is crucial, being the unique dietary source of alkaline precursor constituents, so it is important reason to increase consumption to avoid bone loss during ageing8,48,49. Vegetables and fruit are considered alkaline because of their high mineral content in the form of salts of organic acids. The salts, predominantly potassium based but also calcium and magnesium, generate bicarbonate to balance the acid produced from the rest of the diet20. Consumption of legumes and cereal and bone health Legume and cereal consumption is high in Mediterranean areas. These foods are highly rich in vitamin B, calcium, phytoestrogens and other phytochemicals. Thus, an adequate intake of these foods has been associated with higher bone mineral density, decreased bone loss with ageing, or reduced risk of fracture22. There are data showing that legumes and grains may protect bone metabolism in humans50. It has been showed that the consumption of legumes decreased bone turnover in ovariectomized rats. In a recent study, Park et al.51 showed that a diet containing legumes significantly increased the bone mineral density of the femur and spine, and bone volume of the femur in ovariectomized rats. On the contrary, Rivas and coworkers22 did not find any significant association between legume and cereal intake and bone mineral density in a sample of healthy women from Southern Spain. One explanation could be that the consumption
Nutr Hosp. 2014;29(5):989-996
993
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 994
of this food group was similar in all the subjects studied, so it may be difficult to find any significant differences. In addition non-refined cereals and legumes are acid-producing foods, which may alter the acid-base balance that is associated with negative impact on bone health20.
tors). However, neither the exact benefit nor the exact mechanism of action of fatty acids has been determined yet. Therefore, although there are some clinical evidences linking bone metabolism and dietary lipids, more clinical trials are necessary to prove whether dietary changes or omega-3 supplementation play a major role in bone health and turnover8.
Alcohol effects on bone Conclusion Alcohol and more specifically wine, is an essential component of the Mediterranean diet. There is inconsistent evidence regarding the association between alcohol consumption and bone mineral density (BMD). Tucker et al.52 showed that moderate consumption of alcohol may be beneficial to bone in men and postmenopausal women. However, in men, high liquor intakes (> 2 drinks/d) were associated with significantly lower BMD. The authors concluded that the tendency toward stronger associations between BMD and beer or wine, relative to liquor, suggests that constituents other than ethanol may contribute to bone health. Ying et al.53 describe the associations between total and beverage-specific alcohol intake and bone loss in older men and women. Their data showed that alcohol intake especially red wine might prevent bone loss in older men. However, women consuming excessive alcohol amount, were found to be at higher risk for hip fracture incidence compared to those consuming moderate amounts. This finding is in agreement with results from other relevant investigations in which moderate intake of alcohol was found to increase bone mineral density54. Nevertheless, over and beyond bone mineral density, one cannot oversee the effect of high alcohol consumption on the risk of falling, as well as its association with low body mass index, which is a risk factor for hip fractures. Fish bone health benefits A moderate consumption of fish is recommended for a healthy diet and is also a feature of the Mediterranean diet. Fish is a source of high quality protein; omega-3 fatty acids; vitamins, such as A and D; and minerals, such as selenium, calcium, iodine and zinc55. Many of these nutrients have positive effects on bone health. The positive effects of calcium and vitamin D, which are the most important nutrients for bone health, have long been established. In Spain, fish consumption accounts for 87% of total dietary vitamin D intake. Several studies have shown a potentially beneficial effect of fish intake56,57 against osteoporosis and fracture occurrence. Recently, omega-3 fatty acids, especially eicosapentaenoic acid and docosahexaenoic acid, have been shown to have a beneficial effect on bone health. Several mechanisms have been proposed (affecting bone formation, bone resorption, serum calcium and vitamin D, oxidative stress, and inflammatory media-
994
Nutr Hosp. 2014;29(5):989-996
In conclusion, a limited number of studies have examined the relationship between Mediterranean Diet and bone health, and they have reported conflicting results. On the one hand, adherence to a traditional MeDi has been associated with higher bone mineral density and lower fracture risk. The results of these studies could be attributed to the combined beneficial effects of individual components of the Mediterranean diet. On the contrary, several studies failed to show any association between adherence to the MeDi and indices of bone mass. There is evidence that specific components of this diet may play a role in the prevention of osteoporosis and/or hip fracture occurrence. In this context, an association has been showed between individual key characteristics of MeDi, such as high consumption of fruits, vegetables, and olive oil, as well as moderate to high consumption of fish, and moderate intake of alcohol with reduced incidence of osteoporosis, or reduced fracture occurrence. Further largescale studies are required to clarify the effect of Mediterranean diet on bone health, in order to establish the role of this diet in the prevention of osteoporosis. References 1. Lee YK, Yoon BH, Koo KH. Epidemiology of Osteoporosis and Osteoporotic Fractures in South Korea. Endocrinol Metab 2013; 28 (2): 90-3. 2. De Souza Genaro P, Martini Araujo L. Effect of protein intake on bone and muscle mass in the elderly. Nutr Rev 2010; 68: 616-23. 3. Rivas A, Romero A, Mariscal-Arcas M, Monteagudo C, López G, Lorenzo ML, Ocaña-Peinado FM, Olea-Serrano F. Association between dietary antioxidant quality score (DAQs) and bone mineral density in Spanish women. Nutr Hosp 2012; 27 (6): 1886-93. 4. Rivas A, Romero A, Mariscal M, Monteagudo C, Hernández J, Olea-Serrano F. Validation of questionnaires for the study of food habits and bone mass. Nutr Hosp 2009; 24 (5): 521-8. 5. Park SJ, Joo SE, Min H, Park JK, Kim Y, Kim SS, Ahn Y. Dietary patterns and osteoporosis risk in postmenopausal korean women. Osong Public Health Res Perspect 2012; 3: 199-205. 6. Gravallese EM, Manning C, Tsay A et al. “Synovial tissue in rheumatoid arthritis is a source of osteoclast differentiation factor,” Arthritis and Rheumatism 2000; 43: 250-8. 7. Nakashima T and Takayanagi H. Osteoimmunology: crosstalk between the immune and bone systems. J Clin Immunol 2009; 29 (5): 555-67. 8. Kajarabille N, Díaz-Castro J, Hijano S, López-Frías M, LópezAliaga I, Ochoa JJ. A new insight to bone turnover: role of ω-3 polyunsaturated fatty acids. Scientific World Journal 2013; 589641. 9. Ciprián D, Navarrete-Muñoz EM, Garcia de la Hera M, Giménez-Monzo D, González-Palacios S, Quiles J, Vioque J.
Antonio Romero Pérez and Ana Rivas Velasco
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 995
10. 11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
Mediterranean and Western dietary patterns in adult population of a Mediterranean area; a cluster analysis. Nutr Hosp 2013; 28 (5): 1741-9. Puel C, Coxam V, Davicco MJ. 2007. Mediterranean diet and osteoporosis prevention. Med Sci (Paris) 23: 756-60. Benetou V, Orfanos P, Pettersson-Kymmer U, Bergström U, Svensson O, Johansson I, Berrino F, Tumino R, Borch KB, Lund E, Peeters PH, Grote V, Li K, Altzibar JM, Key T, Boeing H, von Ruesten A, Norat T, Wark PA, Riboli E, Trichopoulou A.Mediterranean diet and incidence of hip fractures in a European cohort. Osteoporos Int 2013; 24 (5): 1587-98. Alacid F, Vaquero-Cristóbal R, Sánchez-Pato A, Muyor JM, López-Miñarro PÁ. Habit based consumptions in the Mediterranean diet and the relationship with anthropometric parameters in young female kayakers. Nutr Hosp 2014; 29 (1): 121-7. Arós F, Corella D, Covas MI, Estruch R, Fiol M, Lapetra J, Gómez-Gracia E, Lamuela-Raventos RM, Martínez A, Martínez-González MA, Pintó X, Portillo Mdel P, Ros E, RuizGutiérrez V, Saez G, Salas-Salvadó J, Serra-Majem L, Tur J; los investigadores PREDIMED. How to publish in The New England Journal of Medicine and not to die while trying it; the PREDIMED experience. Nutr Hosp 2013; 28 (4): 977-9. Sotos Prieto M, Guillen M, Sorlí JV, Asensio EM, Gillem Sáiz P, González JI, Corella D. Meat and fish consumption in a high cardiovascular risk Spanish Mediterranean population. Nutr Hosp 2011; 26 (5): 1033-40. Naska A, Trichopoulou A. Back to the future: The Mediterranean diet paradigm. Nutr Metab Cardiovasc Dis 2013; S09394753 (13) 00302-5. Grao-Cruces A, Nuviala A, Fernández-Martínez A, PorcelGálvez AM, Moral-García JE, Martínez-López EJ. [Adherence to the Mediterranean diet in rural and urban adolescents of southern Spain, life satisfaction, anthropometry, and physical and sedentary activities. Nutr Hosp 2013; 28 (4): 1129-35. Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PW, Felson D, Kiel DP. Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 2002; 76: 245-52. T. Nakashima and H. Takayanagi, “Osteoimmunology: crosstalk between the immune and bone systems. J Clin Immunol 2009; 29 (5): 555-67. Ambroszkiewicz J, Klemarczyk W, Gajewska J, Chełchowska M, Franek E, Laskowska-Klita T. The influence of vegan diet on bone mineral density and biochemical bone turnover markers. Pediatr Endocrinol Diabetes Metab 2010;16 (3): 201-4. Kontogianni MD, Melistas L, Yannakoulia M, Malagaris I, Panagiotakos DB, Yiannakouris N. Association between dietary patterns and indices of bone mass in a sample of Mediterranean women. Nutrition 2009; 25: 165-71. Bullo M, Amigo-Correig P, Márquez-Sandoval F, Babio N, Bulló M, Amigó-Correig P, Márquez-Sandoval F, Babio N, Martínez-González MA,Estruch R, Basora J, Solà R, SalasSalvadó J. Mediterranean diet and high dietary acid load associated with mixed nuts: effect on bone metabolism in elderly subjects. J Am Geriatr Soc 2009: 57 (10): 1789-98. Rivas A, Romero A, Mariscal-Arcas M, Monteagudo C, Feriche B, Lorenzo ML, Olea F. Mediterranean diet and bone mineral density in two age groups of women. Int J Food Sci Nutr 2013; 64 (2): 155-61. Fernández-Real JM, Bulló M, Moreno-Navarrete JM, Ricart W, Ros E, Estruch R, Salas-Salvadó J. A Mediterranean diet enriched with olive oil is associated with higher serum total osteocalcin levels in elderly men at high cardiovascular risk. J Clin Endocrinol Metab 2012; 97 (10): 3792-8. Feart C, Lorrain S, Ginder Coupez V, Samieri C, Letenneur L, Paineau D, Barberger-Gateau P. Adherence to a Mediterranean diet and risk of fractures in French older persons. Osteoporos Int 2013; 24 (12): 3031-41. Martínez-Ramírez MJ, Palma S, Martínez-González MA, Delgado-Martínez AD, de la Fuente C, Delgado-Rodríguez M. Dietary fat intake and the risk of osteoporotic fractures in the elderly. Eur J Clin Nutr 2007; 61: 1114-20.
Adherence to Mediterranean diet and bone health
26. Trichopoulou A, Georgiou E, Bassiakos Y, Lipworth L, Lagiou P, Proukakis C, Trichopoulos D. Energy intake and monounsaturated fat in relation to bone mineral density among women and men in Greece. Prev Med 1997; 26: 395-400. 27. Rivas A, Sanchez-Ortiz A, Jiménez B, García-Moyano J, Lorenzo ML. Phenolic acid content and sensory properties of two Spanish monovarietal virgin olive oils. Eur J Lipid Sci Technol 2013; 115; 621-30. 28. Dai Z Li Y, Quarles LD, Song T, Pan W, Zhou H, Xiao Z. Resveratrol enhances proliferation and osteoblastic differentiation in human mesenchymal stem cells via ER-dependent ERK1/2 activation. Phytomedicine, 14, 806-814. 29. Hagiwara K, Goto T, Araki M, Miyazaki H, Hagiwara H. Olive polyphenol hydroxytyrosol prevents bone loss. Eur J Pharmacol 2011; 662: 78-84. 30. Kim TH, Jung JW, Ha BG, Hong JM, Park EK, Kim HJ, Kim SY. The effects of luteolin on osteoclast differentiation, function in vitro and ovariectomy-induced bone loss. J Nutr Biochem 2011; 22 (1): 8-15. 31. Santiago-Mora R, Casado-Díaz A, De Castro MD, QuesadaGómez JM. Oleuropein enhances osteoblastogenesis and inhibits adipogenesis: the effect on differentiation in stem cells derived from bone marrow. Osteoporos Int 2011; 22 (2): 675-84. 32. Puel C, Mathey J, Agalias A, Kati-Coulibaly S, Mardon J, Obled C, Davicco MJ, Lebecque P, Horcajada MN, Skaltsounis AL, Coxam V. Dose-response study of effect of oleuropein, an olive oil polyphenol, in an ovariectomy/inflammation experimental model of bone loss in the rat. Clin Nutr 2006; 25 (5): 859-68. 33. Puel C, Quintin A, Agalias A, Mathey J, Obled C, Mazur A, et al. Olive oil and its main phenolic micronutrient (oleuropein) prevent inflammation-induced bone loss in the ovariectomised rat. Br J Nut 2004; 92: 119-127. 34. Trzeciakiewicz A, Habauzit V, Horcajada MN. When nutrition interacts with osteoblast function: molecular mechanisms of polyphenols. Nutr Res Rev 2009; 22: 68-81. 35. Li JJ, Huang ZW, Wang RQ, Ma XM, Zhang ZQ, Liu Z, Chen YM, Su YX. Fruit and vegetable intake and bone mass in Chinese adolescents, young and postmenopausal women. Public Health Nutr 2013 Jan; 16 (1): 78-86. 36. Hardcastle AC, Aucott L, Fraser WD, Reid DM, Macdonald HM. Dietary patterns, bone resorption and bone mineral density in early post-menopausal Scottish women. Eur J Clin Nutr 2011; 65: 378-85. 37. Xie HL, Wu BH, Xue WQ, He MG, Fan F, Ouyang WF, Tu SL, Zhu HL, Chen YM. Greater intake of fruit and vegetables is associated with a lower risk of osteoporotic hip fractures in elderly Chinese: a 1: 1 matched case-control study. Osteoporos Int 2013; 24 (11): 2827-36. 38. Tylavsky FA, Holliday K, Danish R, Womack C, Norwood J, Carbone L. 2004. Fruit and vegetable intakes are an independent predictor of bone size in early pubertal children. Am J Clin Nutr 2004; 79: 311-7. 39. Vatanparast H, Baxter-Jones A, Faulkner RA, Bailey DA,Whiting SJ. Positive effects of vegetable and fruit consumption and calcium intake on bone mineral accrual in boys during growth from childhood to adolescence: the University of Saskatchewan Pediatric bone mineral accrual study. Am J Clin Nutr 2005; 82: 700-6. 40. Chen YM, Ho SC,Woo JL. Greater fruit and vegetable intake is associated with increased bone mass among postmenopausal Chinese women. Br J Nutr 2006; 96: 745-51. 41. McGartland CP, Robson PJ, Murray LJ, Cran GW, Savage MJ, Watkins DC, et al. Fruit and vegetable consumption and bone mineral density: the Northern Ireland Young Hearts Project. Am J Clin Nutr 2004; 80: 1019-23. 42. Prynne CJ, Mishra GD, O’Connell MA, Muniz G, Laskey MA, Yan L, et al. 2006. Fruit and vegetable intakes and bone mineral status: a cross sectional study in 5 age and sex cohorts. Am J Clin Nutr 2006; 83: 1420-8. 43. McTiernan A,Wactawski-Wende J,Wu L, Rodabough RJ,Watts NB,Tylavsky F, Women’s Health Initiative Investigators, et al. Low-fat, increased fruit, vegetable, and grain dietary pattern, fractures, and bonemineral density: theWomen’sHealth Initiative
Nutr Hosp. 2014;29(5):989-996
995
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 996
Dietary Modification Trial. Am J Clin Nutr 2009; 89: 1864-76. 44. Prynne CJ, Mishra GD, O’Connell MA, Muniz G, Laskey MA, Yan L, et al. Fruit and vegetable intakes and bone mineral status: a cross sectional study in 5 age and sex cohorts. Am J Clin Nutr 2006; 83: 1420-8. 45. Schulman RC, Weiss AJ, Mechanick JI. Nutrition, bone, and aging: an integrative physiology approach. Curr Osteoporos Rep 2011 Dec; 9 (4): 184-95. 46. Yang Z, Zhang Z, Penniston KL, Binkley N, Tanumihardjo SA. Serum carotenoid concentrations in postmenopausal women from the United States with and without osteoporosis. Int J Vitam Nutr Res 2008; 78: 105-11. 47. Martínez-González MA, Estruch R, et al. Mediterranean diet and high dietary acid load associated with mixed nuts: effect on bone metabolism in elderly subjects. J Am Geriatr Soc 2009; 57: 1789-98. 48. Anandacoomarasamy A, Fransen M, March L. Obesity and the musculoskeletal system. Current Opinion in Rheumatology 2009; 21: 71-7. 49. Elefteriou F, Takeda S, Ebihara K et al. “Serum leptin level is a regulator of bone mass. Proceedings of the National Academy of Sciences of the United States of America 2004; 101: 3258-63. 50. Pérez-López FR, Chedraui P, Haya J, Cuadros JL. Effects of the Mediterranean diet on longevity and age-related morbid conditions. Maturitas 2009; 64: 67-79. 51. Park Y, Moon HJ, Paik DJ, Kim DY. Effect of dietary legumes
996
Nutr Hosp. 2014;29(5):989-996
52.
53.
54.
55.
56.
57.
on bone-specific gene expression in ovariectomized rats. Nutr Res Pract 2013 Jun; 7 (3): 185-91. Tucker KL, Jugdaohsingh R, Powell JJ, Qiao N, Hannan MT, Sripanyakorn S, Cupples LA, Kiel DP. Effects of beer, wine, and liquor intakes on bone mineral density in older men and women. Am J Clin Nutr 2009 Apr; 89 (4): 1188-96. Yin J, Winzenberg T, Quinn S, Giles G, Jones G. Beveragespecific alcohol intake and bone loss in older men and women: a longitudinal study. Eur J Clin Nutr 2011; 65 (4): 526-32. Marrone JA, Maddalozzo GF, Branscum AJ, Hardin K, CialdellaKam L, Philbrick KA, Breggia AC, Rosen CJ, Turner RT, Iwaniec UT. Moderate alcohol intake lowers biochemical markers of bone turnover in postmenopausal women. Menopause 2012 Sep; 19 (9): 974-9. Chen YM, Ho SC, Lam SS. Higher sea fish intake is associated with greater bone mass and lower osteoporosis risk in postmenopausal Chinese women. Osteoporos Int 2010; 21: 939-46. Paunescu AC, Ayotte P, Dewailly E, Dodin S, Pedersen HS, Mulvad G, Côté S. Polyunsaturated fatty acids and calcaneal ultrasound parameters among Inuit women from Nuuk (Greenland): a longitudinal study. Int J Circumpolar Health 2013; 72: 20988. Calderon-Garcia JF, Moran JM, Roncero-Martin R, Rey-Sanchez P, Rodriguez-Velasco FJ, Pedrera-Zamorano JD. Dietary habits, nutrients and bone mass in Spanish premenopausal women: the contribution of fish to better bone health. Nutrients 2012; 5 (1):
Antonio Romero Pérez and Ana Rivas Velasco
Copyright of Nutricion Hospitalaria is the property of Sociedad Espanola de Nutricion Parenteral y Enteral and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
Nutr Hosp. 2014;29(5):989-996 ISSN 0212-1611 • CODEN NUHOEQ S.V.R. 318
Revisión
Adherence to Mediterranean diet and bone health Antonio Romero Pérez1 y Ana Rivas Velasco2 Servicio Andaluz de Salud. Spain. 2Departamento de Nutrición y Bromatología. Facultad de Farmacia. Universidad de Granada. Spain.
1
Abstract Introduction: Several studies have concluded that incidences of osteoporosis and osteoporosis-related fractures vary across the European Union, the lowest incidence being reported in the Mediterranean area. The beneficial effect is mainly attributed to a specific eating pattern. The Mediterranean diet contain a complex array of naturally occurring bioactive molecules with antioxidant, anti-inflammatory and alkalinising properties that may contribute to the bone-sparing effect of the Mediterranean diet. Objective: The purpose of this review is to examine the evidence to date on the effects of Mediterranean diet on bone health. Methods: The search for articles came from extensive research in the following databases: PubMed, Scopus and Web of Science. We used the search terms “Mediterranean diet”, “adherence”, “fruit and vegetable“, “olive oil“, “fish” “legume”, “cereal” “alcohol”, “bone”, “osteoporosis”, “fracture”, and combinations, such as “Mediterranean diet and bone” or “Mediterranean diet and fracture”. Results: A limited number of studies have examined the relationship between Mediterranean Diet and bone health, and they have reported conflicting results. On the one hand, adherence to a traditional MeDi has been associated with higher bone mineral density and lower fracture risk. The results of these studies could be attributed to the combined beneficial effects of individual components of the Mediterranean diet. On the contrary, several studies failed to show any association between adherence to the MeDi and indices of bone mass. Conclusions: Further large-scale studies are required to clarify the effect of Mediterranean diet on bone health, in order to establish the role of this diet in the prevention of osteoporosis.
(Nutr Hosp. 2014;29:989-996) DOI:10.3305/nh.2014.29.5.7332 Key words: Mediterranean diet. Osteoporosis. Bone.
ADHERENCIA A LA DIETA MEDITERRÁNEA Y SALUD ÓSEA Resumen Introducción: Se han encontrado diferencias en los valores de incidencia de osteoporosis y fracturas relacionadas entre los países de la Unión Europea, siendo menor en los países de la zona mediterránea. Este hecho se atribuye principalmente a un patrón de alimentación específica común. La dieta mediterránea contiene un complejo conjunto de componentes bioactivos con propiedades antioxidantes, anti-inflamatorias y alcalinizantes que pueden contribuir al efecto de esta dieta en la salud ósea. Objetivo: El propósito de esta revisión es examinar la evidencia hasta la fecha sobre los efectos de la dieta mediterránea sobre la salud ósea. Métodos: Se realizó una búsqueda en la literatura científica utilizando las siguientes base de datos: PubMed, Scopus and Web of Science. Utilizamos los términos de búsqueda “Dieta Mediterránea”, “adhesión“, “frutas y verduras”, “aceite de oliva“, “pescado” “legumbres”, “cereal”, “alcohol”, “hueso“, “osteoporosis”,”fractura”, y combinaciones, como “Dieta Mediterránea y el hueso“ o “Dieta mediterránea y fracturas“. Resultados: Existe un número limitado de estudios que analicen la relación entre el seguimiento de la Dieta Mediterránea y la salud ósea, mostrando resultados contradictorios. Diversos trabajos han mostrado que la adherencia a una dieta mediterránea tradicional se asociado con una mayor densidad mineral ósea y un menor riesgo de fractura en población adulta. Los resultados de estos estudios podrían atribuirse a un efecto beneficioso combinado de los componentes individuales de la dieta mediterránea. Por el contrario, en otros trabajos no se ha encontrado ninguna asociación entre la adherencia a la dieta mediterránea y los índices de masa ósea. Conclusiones: Se requieren más estudios a gran escala para aclarar el efecto de la dieta mediterránea sobre la salud ósea, con el fin de establecer el papel de la dieta en la prevención de la osteoporosis.
(Nutr Hosp. 2014;29:989-996) DOI:10.3305/nh.2014.29.5.7332 Correspondence: Ana Rivas Velasco. Departamento de Nutrición y Bromatología. Facultad de Farmacia. Universidad de Granada. E-mail: [email protected]
Palabras clave: Dieta mediterránea. Osteoporosis. Hueso.
Recibido: 7-II-2014. 1.ª Revisión: 11-II-2014. Aceptado: 12-III-2014.
989
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 990
Introduction Osteoporosis (OP) is an important worldwide public health concern1 that affects many millions of people around the world and that will take on increasing significance as people live longer and the world s population continues to increase in number2. In addition, osteoporosis related fractures are one of the leading causes of significant morbidity and disability in elderly patients and increases the economic burden on the health care system.The mechanisms involved in osteoporosis pathogenesis are not fully understood3. A reduction in bone density in earlier life is likely to increase the risk of OP and its sequelae in adulthood. It is therefore important to raise awareness among the general population on the need to form and maintain good bone health from childhood through the adoption of healthy habits. OP development is influenced by multiple factors. Bone modelling and remodelling processes are governed not only by heritable traits but also by nutritional, mechanical and hormonal factors4. Besides the aging process, an inadequate diet and sedentary lifestyle can reduce mineralization. Although nutrition is only one of the many factors that influence bone mass and fragility fractures, it is of particular importance to bone health because it is modifiable. Diet can be modified for the maintenance and development of bone mass. Proper nutrient intake has a crucial role in both prevention and treatment of osteoporosis5. The most relevant nutrients to bone health are calcium and phosphorus because they compose roughly 80% to 90% of the mineral content of bone hydroxyapatite; protein is essential because it is incorporated into the organic matrix of bone for collagen structure upon which mineralization occurs; trace elements, and vitamins (e.g., vitamins D and K) are also crucial in carrying out metabolic processes and reactions in bone6,7. Other benefits on bone metabolism derives from bioactive components found basically in vegetables but also some herbs and fruit. Phytochemicals, antioxidants, and other bioactive compounds influence bone metabolism through a variety of mechanisms mainly in reducing oxidative stress and inflammation8. To date, the most consistently followed approach to examine the potential relation between dietary factors and skeletal health was based on particular nutrients such as calcium and vitamin D3. However, people do not eat isolated nutrients but meals consisting of a variety of foods with complex combinations of nutrients and bioactive components. The traditional analysis considering the effect of a few isolated nutrients on bone health misses a lot of information regarding complex or cumulative correlations and interactions between these compounds contained in food. For this reason, there is an increasing interest in the study of dietary patterns that could answer some questions and promote the development of appropriate recommendations for overall dietary habits9 .
990
Nutr Hosp. 2014;29(5):989-996
Several studies have concluded that incidences of osteoporosis and osteoporosis-related fractures vary across the European Union. Conspicuous differences are encountered in the severity of osteoporosis, the lowest incidence being reported in the Mediterranean area10. The beneficial effect is mainly attributed to a specific eating pattern. The Mediterranean diet (MeDi) key characteristics are high intake of vegetables, legumes, fruits and cereals; moderate to high intake of fish; low intake of saturated lipids and high intake of unsaturated lipids, particulary olive oil; low to moderate intake of dairy products, low intake of meat; and modest intake of ethanol, mostly in the form of wine11,12. The Mediterranean diet was introduced to the scientific community by the classic Seven Countries study. Since then data on the association between this diet and cardiovascular disease13,14, cancer and other chronic diseases have been accumulating15,16. However, a limited number of cross-sectional studies have examined the relationship between Mediterranean diet adherence and bone health, and they have reported conflicting results. Therefore, the purpose of this review is to examine the evidence to date on the effects of Mediterranean diet on bone health. Methods The search for articles came from extensive research in the following databases: PubMed, Scopus and Web of Science. We used the search terms “Mediterranean diet”, “adherence”, “fruit and vegetable“, “olive oil“, “fish” “legume”, “cereal” “alcohol”, “bone”, “osteoporosis”, “fracture”, and combinations, such as “Mediterranean diet and bone” or “Mediterranean diet and fracture”. The titles and abstracts of the located documents were initially reviewed and the reference lists of selected papers were searched to identify additional articles. We narrowed the search to studies published in English. Additional publications were identified from references provided in original papers. Results and discussion Adherence to Mediterranean diet and bone health The Mediterranean diet is characterized by a high intake of olive oil, plant products, fish and seafood; a low intake of dairies, meat and meat products; and a moderate ethanol intake15. These food items contain a complex array of naturally occurring bioactive molecules with antioxidant, anti-inflammatory and alkalinising properties that may contribute to the bone-sparing effect of the Mediterranean diet10. Adherence to a dietary pattern close to the Mediterranean diet, have shown to prevent bone disease. Eating habits based on fruit, vegetables, milk, and cereals –that is, similar to those of the Mediterranean
Antonio Romero Pérez and Ana Rivas Velasco
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 991
diet– were proven by the Framingham study to be significantly associated with greater bone mass17. Nakashima and Takayanagi18 studied associations between dietary patterns and bone mineral density in Japanese farmwomen and showed that a “healthy” pattern, described by high intakes of green and dark yellow vegetables, mushrooms, fish and shellfish, and fruit, was positively related to bone mineral density. Furthermore, the effect of vegetarian dietary patterns on skeletal health has been studied; lacto-ovo vegetarians appear to have normal bone mass when compared with omnivores. However, a more recent study reported that the scientific findings support the hypothesis that vegans do have lower bone mineral density than their nonvegan counterparts19. There are few studies that have assessed the effect of the Mediterranean diet on bone health. Besides, the impact of MeDi adherence on bone health remains unclear. In table I are summarized the characteristics of these studies included in relation to where the work was conducted, the number of participants in each study, the methods used to evaluate Mediterranean diet adherence, and the main results. Kontogianni et al.20 described that adherence to a Mediterranean diet evaluated through a Mediterranean Diet Score was not associated with bone mass rates in a sample of adult Greek women, whereas adherence to a dietary pattern close to the Mediterranean diet, i.e., high consumption of fish and olive oil and low red meat intakes, was positively related to bone mass, suggesting the potential bonepreserving properties of this pattern through adult life. An interventional study conducted in Spain21, concluded that a Mediterranean dietary pattern enriched with mixed nuts, does not seem to have any significant effect on bone metabolism in elderly subjects. However the authors pointed out that the sample selection criteria could limit the extrapolation of the findings, as the endpoint of the study was cardiovascular mortality, so the study focused on subjects with a high risk of cardiovascular disease and had already been eating a reasonably good Mediterranean diet pattern for a long time before randomization into the trial21. Recently, Rivas and coworkers22 hypothesized that adherence to the Mediterranean diet measured as a Mediterranean diet score (MDS) has a beneficial effect on bone mineral density in the calcaneus measured by a dual energy X-ray absorptiometry. For the purposes of this study, a sample of healthy women from Southern Spain was chosen. Subjects were grouped into two major groups: a first group consisted of women of reproductive age, and a second group consisted of postmenopausal women. Significant linear trends between the MDS and bone mineral density were observed in all subjects studied. The authors concluded that a varied diet based on Mediterranean diet patterns may be beneficial in the prevention of osteoporosis. Fernandez-Real et al.23 compared the effects of a virgin olive oil enriched Mediterranean diet, a walnut-enriched Mediterranean diet, and a low-
Adherence to Mediterranean diet and bone health
fat diet for two years on osteocalcin and bone formation markers in the blood of men at high risk of cardiovascular disease. The virgin olive oil enriched Mediterranean diet alone was associated with increased serum levels of osteocalcin and the bone remodelling marker procollagen amino-terminal propeptide, suggesting a protective role for this diet in bone health. The potential protective effect of the MeDi against the risk of hip fractures has been evaluated in several studies. Recently, in a large cohort of adults from eight European countries, Benetou et al11 reported an inverse association between adherence to a Mediterraneantype diet and the risk of hip fracture in European older persons. Indeed, in this large cohort of adults enrolled in the EPIC study (N = 188,795 participants, 802 incident hip fractures), higher adherence to the MeDi was associated with a 7% decrease in hip fracture incidence, notably among participants aged 60 years or older and among men in the model adjusted only. On the contrary Feart and coworkers24 showed that greater MeDi adherence was not associated with a decreased risk of fractures in French older persons. There is evidence that specific components of Mediterranean diet may prevent the prevention of osteoporosis and/or hip fracture occurrence. In this context, a summary of the studies that demonstrate this association is shown below. Olive oil and bone Scarce epidemiological literature is available about the association between fat intake and the bone health. Saturated fat (SFA) intake has been reported to be associated with a higher risk of bone loss and osteoporotic fractures25. On the contrary, monounsaturated fat (MUFA) has been reported to have a beneficial effect on bone health25,26. Various epidemiological studies have associated the intake of the monounsaturated fatty acids of olive oil with bone health. A study of male and female adults in Greece26 reported a positive association between the intake of monounsaturated fats and mineral bone density; the authors highlighted the substantially lower incidence of fractures in Greece, where there is high olive oil consumption, than in the USA or North European countries. Rivas et al.4 described in female adults in Spain a significant correlation between the consumption of monounsaturated fatty acids and the mineral density of the heel bone (calcaneus). Besides triglycerides, olive oil contains a wide variety of so-called minor compounds that are of major importance from a chemical and organoleptic standpoint. These include phenolic compounds, which constitute a highly complex fraction formed by numerous substances, some of which are yet to be identified. The known substances include simple phenols, e.g., hydroxytyrosol, tyrosol, caffeic acid, vanillic acid, p-coumaric acid, ferulic acid, and vanillin; flavonoids,
Nutr Hosp. 2014;29(5):989-996
991
992
Nutr Hosp. 2014;29(5):989-996 Adult aged 60 to 80 years at high risk for CVdisease (N=230).
Adult women aged 18-65 years (N=200).
Fernández-real et al. (2012) 23 Spain.
Rivas et al. (2013)22
Method used to evaluate MeDi adherence Results
Mediterranean Diet Score Significant linear trends (Trichopoulou et al., 2003) 22. between MeDi adherence and BMD were observed (p= 0.001).
Three interventional groups: Total osteocalcin increased in the MedDiet+VOO group (p=0.007) low-fat diet, a MedDi in parallel to increased P1NP levels (p=0.01) but not in subjects supplemented with VOO, on the MedDiet+nuts (p=0.32). or MedDi supplemented with nuts.
Three interventional groups: Subjects in MedDi with nuts group had nonsignificantly higher urine low-fat diet, a MedDi free deoxypyridoxine:creatinine ratio (p=0.14). supplemented with VOO, or MedDi supplemented with nuts.
France
Adult aged 67 years Incidence of hip, vertebral and wrist fractures Mediterranean Diet Score Higher MeDi adherence was associated with a non-significant or older (N=1,482). were self-reported every 2 years over 8 years. (Trichopoulou et al., 2003)22. increased risk of fractures at any site.
European Adults aged 35-70 years Incident hip fracture was reported by hip Mediterranean Diet Score Adherence to MeDi was associated with a 7% decrease in hip countries (N= 188,795). and radius fracture registries for a median (Trichopoulou et al., 2003)22. fracture incidence. Association was more evident among men and participants in the of 9 years. older individuals. EPIC study.
Calcaneous BMD by DEXA.
Total circulating osteocalcin Bone markers N-terminal propeptide (P1NP).
Bone formation and resorption markers Bone mass by ultrasound scanning.
MeDi: Mediterranean diet. BMD: bone mineral density. DEXA: Dual-energy X-ray absorptiometry. CV: cardiovascular. VOO: Virgin olive oil.
Feart et al. (2013)24
Benetou et al. (2013)11
Adult aged 60 to 80 at high risk for CVdisease (N=230).
Spain.
Bullo et al. (2009) 21
Spain.
Method for measuring bone mass/fracture risk
Conclusions
Greater MeDi adherence was not associated with a decreased risk of fractures in French older persons.
Increased adherence to MeDi appears to protect against hip fracture occurrence, particularly among men.
MedDi pattern is associated with higher BMD.
Consumption of a Mediterranean diet enriched with virgin olive oil for 2 years is associated with increased serum osteocalcin and P1NP concentrations, suggesting protective effects on bone.
A Mediterranean dietary pattern does not seem to have a much greater effect on bone metabolism biomarker.
Adult women (N=300) Lumbar spine and total BMD by DEXA. Mediterranean Diet Score Adherence to MedDi was not associated with indices of bone mass. Adherence to a MedDi was not associated (Trichopoulou et al., 2003) 22. Consumption of fish, olive oil and low intake of red meat was associated with indices of bone mass. with lumbar spine BMD (p = 0.017) and total body BMD (p = 0.048)
Subjects
Greece.
Country
Kontogani et al. (2010)20
Reference
Tabla I Description of the studies that have assessed the effect of the Mediterranean diet on bone health
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 992
Antonio Romero Pérez and Ana Rivas Velasco
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 993
e.g., luteolin and apigenin; and other more complex compounds such as those derived from oleuropein, ligstroside, ligustaloside27. Numerous potential health benefits of the phenolic compounds of olive oil have been reported, but their role in the prevention of bone diseases (e.g., osteoporosis) has been less well studied. Researchers have shown the phenolic compounds in different vegetables species can modulate the functions of osteoblastic cells, including their proliferative capacity and maturation, by increasing alkaline phosphatase activity and the deposit of calcium ions in the extracellular matrix28-30. Oleuropein, the main phenolic compound in olive-tree leaves, together with virgin olive oil and olives, was proved to be effective in a rat model of senile osteoporosis with a dosage of 150 mg/kg diet. In addition oleuropein shifts the differentiation of mesenchymal stromal cells in favour of osteoblastogenesis suggesting that oleuropein intake might have preventive effects against the bone loss associated with osteoporosis and aging31. The main phenolic compounds in virgin olive oil are tyrosol and hydroxytyrosol. Their administration in the diet at doses of 0.017% prevented the inflammation-induced bone mass loss in ovariectomized rats in a model of senile osteoporosis and increased their osteoblast activity, as evidenced by their elevated plasma osteocalcin levels32,33. Finally, luteolin, a flavonoid present in VOO, lessens bone mass loss in postmenopausal osteoporosis by reducing osteoclast differentiation and function34. Intake of fruits and vegetables: implications for bone health Fruit and vegetable consumption is a common feature of the Mediterranean diet. Recent studies have focused on the effects of fruit and vegetable intakes on bone health35,36. Fruit and vegetable intake has been associated with increased bone mineral density or reduced fracture risk37. Larger bone size in early pubertal children and adolescents38-40, and better bone mass in adult men and women have been associated with fruit and vegetable consumption41,42. In addition, it has been demonstrated that a dietary intervention based on low fat and increased fruit, vegetable, and grain intake reduced moderately the risk of multiple falls and slightly lower hip BMD43. The mechanism whereby fruit and vegetables may affect bone is not clear and may be multifactorial44. Fruits and vegetables might affect bone health via the effects of several components in these foods, such as minerals (e.g., calcium, potassium, and magnesium), vitamins (e.g., vitamin K and C), phytochemicals (e.g., phytoestrogens), and oligosaccharides (especially inulin-type fructans), either through their effect on calcium absorption or their involvement in the bone remodeling sequence, could mediate this association11,45. In addition, fruits and vegetables contain many
Adherence to Mediterranean diet and bone health
different antioxidant components. Several lines of evidence suggest a tight association between oxidative stress and the pathogenesis of osteoporosis in humans. It has been shown that osteoporotic women have lower serum antioxidants levels as compared with controls12,46. Recently, Rivas et al.3 demonstrated that the overall dietary antioxidant intake was significantly associated with bone mineral density in adult women. It should be taken into account that a higher dietary acid load is believed to result in bone mineral dissolution and greater bone resorption, and a diet rich in fruit and vegetables may result in a more alkaline environment, which has been proven to reduce urinary calcium excretion43. The low grade metabolic acidosis induced by the modern diet is exacerbated during ageing when renal function begins to decline requiring the body’s skeletal reserves to be called upon to relinquish bicarbonate to produce alkaline buffers needed to continuously balance the acid load.Typical diets are acidic because predominantly acid (hydrogen ions) rather than base (bicarbonate) is created during the metabolism of the daily food intake. Acid forming grains and high protein food derived from animal origin (meat, fish, and eggs) contain sulphur-based amino acids, methionine, and cysteine which create acid when metabolized. Alkaline forming foods contain potassium salts which can be broken down to make alkaline buffers47. Fruit/vegetables influence on acid-base balance is crucial, being the unique dietary source of alkaline precursor constituents, so it is important reason to increase consumption to avoid bone loss during ageing8,48,49. Vegetables and fruit are considered alkaline because of their high mineral content in the form of salts of organic acids. The salts, predominantly potassium based but also calcium and magnesium, generate bicarbonate to balance the acid produced from the rest of the diet20. Consumption of legumes and cereal and bone health Legume and cereal consumption is high in Mediterranean areas. These foods are highly rich in vitamin B, calcium, phytoestrogens and other phytochemicals. Thus, an adequate intake of these foods has been associated with higher bone mineral density, decreased bone loss with ageing, or reduced risk of fracture22. There are data showing that legumes and grains may protect bone metabolism in humans50. It has been showed that the consumption of legumes decreased bone turnover in ovariectomized rats. In a recent study, Park et al.51 showed that a diet containing legumes significantly increased the bone mineral density of the femur and spine, and bone volume of the femur in ovariectomized rats. On the contrary, Rivas and coworkers22 did not find any significant association between legume and cereal intake and bone mineral density in a sample of healthy women from Southern Spain. One explanation could be that the consumption
Nutr Hosp. 2014;29(5):989-996
993
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 994
of this food group was similar in all the subjects studied, so it may be difficult to find any significant differences. In addition non-refined cereals and legumes are acid-producing foods, which may alter the acid-base balance that is associated with negative impact on bone health20.
tors). However, neither the exact benefit nor the exact mechanism of action of fatty acids has been determined yet. Therefore, although there are some clinical evidences linking bone metabolism and dietary lipids, more clinical trials are necessary to prove whether dietary changes or omega-3 supplementation play a major role in bone health and turnover8.
Alcohol effects on bone Conclusion Alcohol and more specifically wine, is an essential component of the Mediterranean diet. There is inconsistent evidence regarding the association between alcohol consumption and bone mineral density (BMD). Tucker et al.52 showed that moderate consumption of alcohol may be beneficial to bone in men and postmenopausal women. However, in men, high liquor intakes (> 2 drinks/d) were associated with significantly lower BMD. The authors concluded that the tendency toward stronger associations between BMD and beer or wine, relative to liquor, suggests that constituents other than ethanol may contribute to bone health. Ying et al.53 describe the associations between total and beverage-specific alcohol intake and bone loss in older men and women. Their data showed that alcohol intake especially red wine might prevent bone loss in older men. However, women consuming excessive alcohol amount, were found to be at higher risk for hip fracture incidence compared to those consuming moderate amounts. This finding is in agreement with results from other relevant investigations in which moderate intake of alcohol was found to increase bone mineral density54. Nevertheless, over and beyond bone mineral density, one cannot oversee the effect of high alcohol consumption on the risk of falling, as well as its association with low body mass index, which is a risk factor for hip fractures. Fish bone health benefits A moderate consumption of fish is recommended for a healthy diet and is also a feature of the Mediterranean diet. Fish is a source of high quality protein; omega-3 fatty acids; vitamins, such as A and D; and minerals, such as selenium, calcium, iodine and zinc55. Many of these nutrients have positive effects on bone health. The positive effects of calcium and vitamin D, which are the most important nutrients for bone health, have long been established. In Spain, fish consumption accounts for 87% of total dietary vitamin D intake. Several studies have shown a potentially beneficial effect of fish intake56,57 against osteoporosis and fracture occurrence. Recently, omega-3 fatty acids, especially eicosapentaenoic acid and docosahexaenoic acid, have been shown to have a beneficial effect on bone health. Several mechanisms have been proposed (affecting bone formation, bone resorption, serum calcium and vitamin D, oxidative stress, and inflammatory media-
994
Nutr Hosp. 2014;29(5):989-996
In conclusion, a limited number of studies have examined the relationship between Mediterranean Diet and bone health, and they have reported conflicting results. On the one hand, adherence to a traditional MeDi has been associated with higher bone mineral density and lower fracture risk. The results of these studies could be attributed to the combined beneficial effects of individual components of the Mediterranean diet. On the contrary, several studies failed to show any association between adherence to the MeDi and indices of bone mass. There is evidence that specific components of this diet may play a role in the prevention of osteoporosis and/or hip fracture occurrence. In this context, an association has been showed between individual key characteristics of MeDi, such as high consumption of fruits, vegetables, and olive oil, as well as moderate to high consumption of fish, and moderate intake of alcohol with reduced incidence of osteoporosis, or reduced fracture occurrence. Further largescale studies are required to clarify the effect of Mediterranean diet on bone health, in order to establish the role of this diet in the prevention of osteoporosis. References 1. Lee YK, Yoon BH, Koo KH. Epidemiology of Osteoporosis and Osteoporotic Fractures in South Korea. Endocrinol Metab 2013; 28 (2): 90-3. 2. De Souza Genaro P, Martini Araujo L. Effect of protein intake on bone and muscle mass in the elderly. Nutr Rev 2010; 68: 616-23. 3. Rivas A, Romero A, Mariscal-Arcas M, Monteagudo C, López G, Lorenzo ML, Ocaña-Peinado FM, Olea-Serrano F. Association between dietary antioxidant quality score (DAQs) and bone mineral density in Spanish women. Nutr Hosp 2012; 27 (6): 1886-93. 4. Rivas A, Romero A, Mariscal M, Monteagudo C, Hernández J, Olea-Serrano F. Validation of questionnaires for the study of food habits and bone mass. Nutr Hosp 2009; 24 (5): 521-8. 5. Park SJ, Joo SE, Min H, Park JK, Kim Y, Kim SS, Ahn Y. Dietary patterns and osteoporosis risk in postmenopausal korean women. Osong Public Health Res Perspect 2012; 3: 199-205. 6. Gravallese EM, Manning C, Tsay A et al. “Synovial tissue in rheumatoid arthritis is a source of osteoclast differentiation factor,” Arthritis and Rheumatism 2000; 43: 250-8. 7. Nakashima T and Takayanagi H. Osteoimmunology: crosstalk between the immune and bone systems. J Clin Immunol 2009; 29 (5): 555-67. 8. Kajarabille N, Díaz-Castro J, Hijano S, López-Frías M, LópezAliaga I, Ochoa JJ. A new insight to bone turnover: role of ω-3 polyunsaturated fatty acids. Scientific World Journal 2013; 589641. 9. Ciprián D, Navarrete-Muñoz EM, Garcia de la Hera M, Giménez-Monzo D, González-Palacios S, Quiles J, Vioque J.
Antonio Romero Pérez and Ana Rivas Velasco
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 995
10. 11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
Mediterranean and Western dietary patterns in adult population of a Mediterranean area; a cluster analysis. Nutr Hosp 2013; 28 (5): 1741-9. Puel C, Coxam V, Davicco MJ. 2007. Mediterranean diet and osteoporosis prevention. Med Sci (Paris) 23: 756-60. Benetou V, Orfanos P, Pettersson-Kymmer U, Bergström U, Svensson O, Johansson I, Berrino F, Tumino R, Borch KB, Lund E, Peeters PH, Grote V, Li K, Altzibar JM, Key T, Boeing H, von Ruesten A, Norat T, Wark PA, Riboli E, Trichopoulou A.Mediterranean diet and incidence of hip fractures in a European cohort. Osteoporos Int 2013; 24 (5): 1587-98. Alacid F, Vaquero-Cristóbal R, Sánchez-Pato A, Muyor JM, López-Miñarro PÁ. Habit based consumptions in the Mediterranean diet and the relationship with anthropometric parameters in young female kayakers. Nutr Hosp 2014; 29 (1): 121-7. Arós F, Corella D, Covas MI, Estruch R, Fiol M, Lapetra J, Gómez-Gracia E, Lamuela-Raventos RM, Martínez A, Martínez-González MA, Pintó X, Portillo Mdel P, Ros E, RuizGutiérrez V, Saez G, Salas-Salvadó J, Serra-Majem L, Tur J; los investigadores PREDIMED. How to publish in The New England Journal of Medicine and not to die while trying it; the PREDIMED experience. Nutr Hosp 2013; 28 (4): 977-9. Sotos Prieto M, Guillen M, Sorlí JV, Asensio EM, Gillem Sáiz P, González JI, Corella D. Meat and fish consumption in a high cardiovascular risk Spanish Mediterranean population. Nutr Hosp 2011; 26 (5): 1033-40. Naska A, Trichopoulou A. Back to the future: The Mediterranean diet paradigm. Nutr Metab Cardiovasc Dis 2013; S09394753 (13) 00302-5. Grao-Cruces A, Nuviala A, Fernández-Martínez A, PorcelGálvez AM, Moral-García JE, Martínez-López EJ. [Adherence to the Mediterranean diet in rural and urban adolescents of southern Spain, life satisfaction, anthropometry, and physical and sedentary activities. Nutr Hosp 2013; 28 (4): 1129-35. Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PW, Felson D, Kiel DP. Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 2002; 76: 245-52. T. Nakashima and H. Takayanagi, “Osteoimmunology: crosstalk between the immune and bone systems. J Clin Immunol 2009; 29 (5): 555-67. Ambroszkiewicz J, Klemarczyk W, Gajewska J, Chełchowska M, Franek E, Laskowska-Klita T. The influence of vegan diet on bone mineral density and biochemical bone turnover markers. Pediatr Endocrinol Diabetes Metab 2010;16 (3): 201-4. Kontogianni MD, Melistas L, Yannakoulia M, Malagaris I, Panagiotakos DB, Yiannakouris N. Association between dietary patterns and indices of bone mass in a sample of Mediterranean women. Nutrition 2009; 25: 165-71. Bullo M, Amigo-Correig P, Márquez-Sandoval F, Babio N, Bulló M, Amigó-Correig P, Márquez-Sandoval F, Babio N, Martínez-González MA,Estruch R, Basora J, Solà R, SalasSalvadó J. Mediterranean diet and high dietary acid load associated with mixed nuts: effect on bone metabolism in elderly subjects. J Am Geriatr Soc 2009: 57 (10): 1789-98. Rivas A, Romero A, Mariscal-Arcas M, Monteagudo C, Feriche B, Lorenzo ML, Olea F. Mediterranean diet and bone mineral density in two age groups of women. Int J Food Sci Nutr 2013; 64 (2): 155-61. Fernández-Real JM, Bulló M, Moreno-Navarrete JM, Ricart W, Ros E, Estruch R, Salas-Salvadó J. A Mediterranean diet enriched with olive oil is associated with higher serum total osteocalcin levels in elderly men at high cardiovascular risk. J Clin Endocrinol Metab 2012; 97 (10): 3792-8. Feart C, Lorrain S, Ginder Coupez V, Samieri C, Letenneur L, Paineau D, Barberger-Gateau P. Adherence to a Mediterranean diet and risk of fractures in French older persons. Osteoporos Int 2013; 24 (12): 3031-41. Martínez-Ramírez MJ, Palma S, Martínez-González MA, Delgado-Martínez AD, de la Fuente C, Delgado-Rodríguez M. Dietary fat intake and the risk of osteoporotic fractures in the elderly. Eur J Clin Nutr 2007; 61: 1114-20.
Adherence to Mediterranean diet and bone health
26. Trichopoulou A, Georgiou E, Bassiakos Y, Lipworth L, Lagiou P, Proukakis C, Trichopoulos D. Energy intake and monounsaturated fat in relation to bone mineral density among women and men in Greece. Prev Med 1997; 26: 395-400. 27. Rivas A, Sanchez-Ortiz A, Jiménez B, García-Moyano J, Lorenzo ML. Phenolic acid content and sensory properties of two Spanish monovarietal virgin olive oils. Eur J Lipid Sci Technol 2013; 115; 621-30. 28. Dai Z Li Y, Quarles LD, Song T, Pan W, Zhou H, Xiao Z. Resveratrol enhances proliferation and osteoblastic differentiation in human mesenchymal stem cells via ER-dependent ERK1/2 activation. Phytomedicine, 14, 806-814. 29. Hagiwara K, Goto T, Araki M, Miyazaki H, Hagiwara H. Olive polyphenol hydroxytyrosol prevents bone loss. Eur J Pharmacol 2011; 662: 78-84. 30. Kim TH, Jung JW, Ha BG, Hong JM, Park EK, Kim HJ, Kim SY. The effects of luteolin on osteoclast differentiation, function in vitro and ovariectomy-induced bone loss. J Nutr Biochem 2011; 22 (1): 8-15. 31. Santiago-Mora R, Casado-Díaz A, De Castro MD, QuesadaGómez JM. Oleuropein enhances osteoblastogenesis and inhibits adipogenesis: the effect on differentiation in stem cells derived from bone marrow. Osteoporos Int 2011; 22 (2): 675-84. 32. Puel C, Mathey J, Agalias A, Kati-Coulibaly S, Mardon J, Obled C, Davicco MJ, Lebecque P, Horcajada MN, Skaltsounis AL, Coxam V. Dose-response study of effect of oleuropein, an olive oil polyphenol, in an ovariectomy/inflammation experimental model of bone loss in the rat. Clin Nutr 2006; 25 (5): 859-68. 33. Puel C, Quintin A, Agalias A, Mathey J, Obled C, Mazur A, et al. Olive oil and its main phenolic micronutrient (oleuropein) prevent inflammation-induced bone loss in the ovariectomised rat. Br J Nut 2004; 92: 119-127. 34. Trzeciakiewicz A, Habauzit V, Horcajada MN. When nutrition interacts with osteoblast function: molecular mechanisms of polyphenols. Nutr Res Rev 2009; 22: 68-81. 35. Li JJ, Huang ZW, Wang RQ, Ma XM, Zhang ZQ, Liu Z, Chen YM, Su YX. Fruit and vegetable intake and bone mass in Chinese adolescents, young and postmenopausal women. Public Health Nutr 2013 Jan; 16 (1): 78-86. 36. Hardcastle AC, Aucott L, Fraser WD, Reid DM, Macdonald HM. Dietary patterns, bone resorption and bone mineral density in early post-menopausal Scottish women. Eur J Clin Nutr 2011; 65: 378-85. 37. Xie HL, Wu BH, Xue WQ, He MG, Fan F, Ouyang WF, Tu SL, Zhu HL, Chen YM. Greater intake of fruit and vegetables is associated with a lower risk of osteoporotic hip fractures in elderly Chinese: a 1: 1 matched case-control study. Osteoporos Int 2013; 24 (11): 2827-36. 38. Tylavsky FA, Holliday K, Danish R, Womack C, Norwood J, Carbone L. 2004. Fruit and vegetable intakes are an independent predictor of bone size in early pubertal children. Am J Clin Nutr 2004; 79: 311-7. 39. Vatanparast H, Baxter-Jones A, Faulkner RA, Bailey DA,Whiting SJ. Positive effects of vegetable and fruit consumption and calcium intake on bone mineral accrual in boys during growth from childhood to adolescence: the University of Saskatchewan Pediatric bone mineral accrual study. Am J Clin Nutr 2005; 82: 700-6. 40. Chen YM, Ho SC,Woo JL. Greater fruit and vegetable intake is associated with increased bone mass among postmenopausal Chinese women. Br J Nutr 2006; 96: 745-51. 41. McGartland CP, Robson PJ, Murray LJ, Cran GW, Savage MJ, Watkins DC, et al. Fruit and vegetable consumption and bone mineral density: the Northern Ireland Young Hearts Project. Am J Clin Nutr 2004; 80: 1019-23. 42. Prynne CJ, Mishra GD, O’Connell MA, Muniz G, Laskey MA, Yan L, et al. 2006. Fruit and vegetable intakes and bone mineral status: a cross sectional study in 5 age and sex cohorts. Am J Clin Nutr 2006; 83: 1420-8. 43. McTiernan A,Wactawski-Wende J,Wu L, Rodabough RJ,Watts NB,Tylavsky F, Women’s Health Initiative Investigators, et al. Low-fat, increased fruit, vegetable, and grain dietary pattern, fractures, and bonemineral density: theWomen’sHealth Initiative
Nutr Hosp. 2014;29(5):989-996
995
05. ADHERENCE_01. Interacción 30/04/14 09:38 Página 996
Dietary Modification Trial. Am J Clin Nutr 2009; 89: 1864-76. 44. Prynne CJ, Mishra GD, O’Connell MA, Muniz G, Laskey MA, Yan L, et al. Fruit and vegetable intakes and bone mineral status: a cross sectional study in 5 age and sex cohorts. Am J Clin Nutr 2006; 83: 1420-8. 45. Schulman RC, Weiss AJ, Mechanick JI. Nutrition, bone, and aging: an integrative physiology approach. Curr Osteoporos Rep 2011 Dec; 9 (4): 184-95. 46. Yang Z, Zhang Z, Penniston KL, Binkley N, Tanumihardjo SA. Serum carotenoid concentrations in postmenopausal women from the United States with and without osteoporosis. Int J Vitam Nutr Res 2008; 78: 105-11. 47. Martínez-González MA, Estruch R, et al. Mediterranean diet and high dietary acid load associated with mixed nuts: effect on bone metabolism in elderly subjects. J Am Geriatr Soc 2009; 57: 1789-98. 48. Anandacoomarasamy A, Fransen M, March L. Obesity and the musculoskeletal system. Current Opinion in Rheumatology 2009; 21: 71-7. 49. Elefteriou F, Takeda S, Ebihara K et al. “Serum leptin level is a regulator of bone mass. Proceedings of the National Academy of Sciences of the United States of America 2004; 101: 3258-63. 50. Pérez-López FR, Chedraui P, Haya J, Cuadros JL. Effects of the Mediterranean diet on longevity and age-related morbid conditions. Maturitas 2009; 64: 67-79. 51. Park Y, Moon HJ, Paik DJ, Kim DY. Effect of dietary legumes
996
Nutr Hosp. 2014;29(5):989-996
52.
53.
54.
55.
56.
57.
on bone-specific gene expression in ovariectomized rats. Nutr Res Pract 2013 Jun; 7 (3): 185-91. Tucker KL, Jugdaohsingh R, Powell JJ, Qiao N, Hannan MT, Sripanyakorn S, Cupples LA, Kiel DP. Effects of beer, wine, and liquor intakes on bone mineral density in older men and women. Am J Clin Nutr 2009 Apr; 89 (4): 1188-96. Yin J, Winzenberg T, Quinn S, Giles G, Jones G. Beveragespecific alcohol intake and bone loss in older men and women: a longitudinal study. Eur J Clin Nutr 2011; 65 (4): 526-32. Marrone JA, Maddalozzo GF, Branscum AJ, Hardin K, CialdellaKam L, Philbrick KA, Breggia AC, Rosen CJ, Turner RT, Iwaniec UT. Moderate alcohol intake lowers biochemical markers of bone turnover in postmenopausal women. Menopause 2012 Sep; 19 (9): 974-9. Chen YM, Ho SC, Lam SS. Higher sea fish intake is associated with greater bone mass and lower osteoporosis risk in postmenopausal Chinese women. Osteoporos Int 2010; 21: 939-46. Paunescu AC, Ayotte P, Dewailly E, Dodin S, Pedersen HS, Mulvad G, Côté S. Polyunsaturated fatty acids and calcaneal ultrasound parameters among Inuit women from Nuuk (Greenland): a longitudinal study. Int J Circumpolar Health 2013; 72: 20988. Calderon-Garcia JF, Moran JM, Roncero-Martin R, Rey-Sanchez P, Rodriguez-Velasco FJ, Pedrera-Zamorano JD. Dietary habits, nutrients and bone mass in Spanish premenopausal women: the contribution of fish to better bone health. Nutrients 2012; 5 (1):
Antonio Romero Pérez and Ana Rivas Velasco
Copyright of Nutricion Hospitalaria is the property of Sociedad Espanola de Nutricion Parenteral y Enteral and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
![[Adherence to the Mediterranean diet of future teachers].](/assets/img/hold.png)
